Stochastic properties of processive cytidine DNA deaminases AID and APOBEC3G

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 364, Issue 1517, 2009, Pages 583-593

  Chelico, Linda ^a   Pham, Phuong ^a   Goodman, Myron F ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

Activation induced (cytidine) deaminase phosphorylation; Class switch recombination; Deamination spectrum; Processivity; Somatic hypermutation; Transcription

Indexed keywords

ANTIBODY; DNA; ENZYME ACTIVITY; STOCHASTICITY;

EID: 60049097628     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2008.0195     Document Type: Conference Paper

References (52)

1. Basu, U., Chaudhuri, J., Alpert, C., Dutt, S., Ranganath, S., Li, G., Schrum, J. P., Manis, J. P. & Alt, F. W. 2005 The AID antibody diversification enzyme is regulated by protein kinase A phosphorylation. Nature 438, 508-511. (doi:10.1038/nature04255)
2. Basu, U., Chaudhuri, J., Phan, R. T., Datta, A. & Alt, F. W. 2007 Regulation of activation induced deaminase via phosphorylation. Adv. Exp. Med. Biol. 596, 129-137. (doi:10.1007/0-387-46530-8-11)
3. Beale, R. C., Petersen-Mahrt, S. K., Watt, I. N., Harris, R. S., Rada, C. & Neuberger, M. S. 2004 Comparison of the differential context-dependence of DNA deamination by APOBEC enzymes: correlation with mutation spectra in vivo. J. Mol. Biol. 337, 585-596. (doi:10.1016/j.jmb.2004.01.046)
4. Bennett, S. E., Sanderson, R. J. & Mosbaugh, D. W. 1995 Processivity of Escherichia coli and rat liver mitochondrial uracil-DNA glycosylase is affected by NaCl concentration. Biochemistry 34, 6109-6119. (doi:10.1021/bi00018a014)
5. Berg, O. G., Winter, R. B. & von Hippel, P. H. 1981 Diffusion-driven mechanisms of protein translocation on nucleic acids. 1. Models and theory. Biochemistry 20, 6929-6948. (doi:10.1021/bi00527a028)
6. Besmer, E., Market, E. & Papavasiliou, F. N. 2006 The transcription elongation complex directs activation-induced cytidine deaminase-mediated DNA deamination. Mol. Cell. Biol. 26, 4378-4385. (doi:10.1128/MCB. 02375-05)
7. Bishop, K. N., Holmes, R. K., Sheehy, A. M., Davidson, N. O., Cho, S. J. & Malim, M. H. 2004 Cytidine deamination of retroviral DNA by diverse APOBEC proteins. Curr. Biol. 14, 1392-1396. (doi:10.1016/j.cub.2004.06. 057)
8. Bransteitter, R., Pham, P., Calabrese, P. & Goodman, M. F. 2004 Biochemical analysis of hypermutational targeting by wild type and mutant activation-induced cytidine deaminase. J. Biol. Chem. 279, 51 612-51 621. (doi:10.1074/jbc.M408135200)
9. Carey, D. C. & Strauss, P. R. 1999 Human apurinic/apyrimidinic endonuclease is processive. Biochemistry 38, 16 553-16 560. (doi:10.1021/bi9907429)
10. Chaudhuri, J., Khuong, C. & Alt, F. W. 2004 Replication protein A interacts with AID to promote deamination of somatic hypermutation targets. Nature 430, 992-998. (doi:10.1038/nature02821)
11. Chaudhuri, J. et al. 2007 Evolution of the immunoglobulin heavy chain class switch recombination mechanism. Adv. Immunol. 94, 157-214. (doi:10.1016/s0065-2776(06)94006-1)
12. Chelico, L., Pham, P., Calabrese, P. & Goodman, M. F. 2006 APOBEC3G DNA deaminase acts processively 3′ → 5′ on single-stranded DNA. Nat. Struct. Mol. Biol. 13, 392-399. (doi:10.1038/nsmb1086)
13. Chelico, L., Sacho, E. J., Erie, D. A.& Goodman, M. F. 2008A model for oligomeric regulation of APOBEC3G cytosine deaminase-dependent restriction of HIV. J. Biol. Chem. 283, 13 780-13 791. (doi:10.1074/jbc. M801004200)
14. Chiu, Y. L. & Greene, W. C. 2008 The APOBEC3 cytidine deaminases: an innate defensive network opposing exogenous retroviruses and endogenous retroelements. Annu. Rev. Immunol. 26, 317-353. (doi:10.1146/annurev.immunol.26.021607.090350)
15. Creighton, S., Bloom, L. B. & Goodman, M. F. 1995 Gel fidelity assay measuring nucleotide misinsertion, exonucleolytic proofreading, and lesion bypass efficiencies. Methods Enzymol. 262, 232-256. (doi:10.1016/0076-6879(95)62021-4)
16. Di Noia, J. M. & Neuberger, M. S. 2007 Molecular mechanisms of antibody somatic hypermutation. Annu. Rev. Biochem. 76, 1-22. (doi:10.1146/annurev.biochem.76.061705.090740)
17. Dowd, D. R. & Lloyd, R. S. 1990 Biological significance of facilitated diffusion in protein-DNA interactions. Applications to T4 endonuclease V-initiated DNA repair. J. Biol. Chem. 265, 3424-3431.
18. Durandy, A., Taubenheim, N., Peron, S. & Fischer, A. 2007 Pathophysiology of B-cell intrinsic immunoglobulin class switch recombination deficiencies. Adv. Immunol. 94, 275-306. (doi:10.1016/s0065- 2776(06)94009-7)
19. Halford, S. E. & Marko, J. F. 2004 How do site-specific DNA-binding proteins find their targets? Nucleic Acids Res. 32, 3040-3052. (doi:10.1093/nar/gkh624)
20. Harris, R. S. & Liddament, M. T. 2004 Retroviral restriction by APOBEC proteins. Nat. Rev. Immunol. 4, 868-877. (doi:10.1038/nri1489)
21. Higley, M. & Lloyd, R. S. 1993 Processivity of uracil DNA glycosylase. Mutat. Res. 294, 109-116.
22. Jack, W. E., Terry, B. J. & Modrich, P. 1982 Involvement of outside DNA sequences in the major kinetic path by which EcoRI endonuclease locates and leaves its recognition sequence. Proc. Natl Acad. Sci. USA 79, 4010-4014. (doi:10.1073/pnas.79.13.4010)
23. Maizels, N. 1995 Somatic hypermutation: how many mechanisms diversify V region sequences? Cell 83, 9-12. (doi:10.1016/0092-8674(95)90227- 9)
24. McBride, K. M., Gazumyan, A., Woo, E. M., Barreto, V. M., Robbiani, D. F., Chait, B. T. & Nussenzweig, M. C. 2006 Regulation of hypermutation by activation-induced cytidine deaminase phosphorylation. Proc. Natl Acad. Sci. USA 103, 8798-8803. (doi:10.1073/pnas.0603272103)
25. Milstein, C. 1987 Diversity and the genesis of high affinity antibodies. Biochem. Soc. Trans. 15, 779-787.
26. Mulder, L. C., Harari, A. & Simon, V. 2008 Cytidine deamination induced HIV-1 drug resistance. Proc. Natl Acad. Sci. USA 105, 5501-5506. (doi:10.1073/pnas.0710190105)
27. Muramatsu, M., Kinoshita, K., Fagarasan, S., Yamada, S., Shinkai, Y. & Honjo, T. 2000 Class switch recombination and hypermutation require activation-induced cytidine deaminase (AID), a potential RNA editing enzyme. Cell 102, 553-563. (doi:10.1016/S0092-8674(00)00078-7)
28. Pasqualucci, L., Kitaura, Y., Gu, H. & Dalla-Favera, R. 2006 PKA-mediated phosphorylation regulates the function of activation-induced deaminase (AID) in B cells. Proc. Natl Acad. Sci. USA 103, 395-400. (doi:10.1073/pnas.0509969103)
29. Peled, J. U., Kuang, F. L., Iglesias-Ussel, M. D., Roa, S., Kalis, S. L., Goodman, M. F. & Scharff, M. D. 2008 The biochemistry of somatic hypermutation. Annu. Rev. Immunol. 26, 481-511. (doi:10.1146/annurev.immunol.26.021607.090236)
30. Peters, A. & Storb, U. 1996 Somatic hypermutation of immunoglobulin genes is linked to transcription initiation. Immunity 4, 57-65. (doi:10.1016/S1074-7613(00)80298-8)
31. Pham, P., Bransteitter, R., Petruska, J. & Goodman, M. F. 2003 Processive AID-catalysed cytosine deamination on single-stranded DNA simulates somatic hypermutation. Nature 424, 103-107. (doi:10.1038/ nature01760)
32. Pham, P., Bransteitter, R. & Goodman, M. F. 2005 Reward versus risk: DNA cytidine deaminases triggering immunity and disease. Biochemistry 44, 2703-2715. (doi:10.1021/bi047481+)
33. Pham, P., Chelico, L. & Goodman, M. F. 2007 DNA deaminases AID and APOBEC3G act processively on single-stranded DNA. DNA Repair (Amst.) 6, 689-692. (doi:10.1016/j.dnarep.2007.01.001)
34. Pham, P., Smolka, M. B., Calabrese, P., Landolph, A., Zhang, K., Zhou, H. & Goodman, M. F. 2008 Impact of phosphorylation and phosphorylation-null mutants on the activity and deamination specificity of activation-induced cytidine deaminase. J. Biol. Chem. 283, 17 428-17 439. (doi:10.1074/jbc.M802121200)
35. Pillai, S. K., Wong, J. K. & Barbour, J. D. 2008 Turning up the volume on mutational pressure: is more of a good thing always better? (A case study of HIV-1 Vif and APOBEC3). Retrovirology 5, 26. (doi:10.1186/1742-4690-5-26)
36. Prochnow, C., Bransteitter, R., Klein, M. G., Goodman, M. F. & Chen, X. S. 2007 The APOBEC-2 crystal structure and functional implications for the deaminase AID. Nature 445, 447-451. (doi:10.1038/nature05492)
37. Rada, C., Di Noia, J. M. & Neuberger, M. S. 2004 Mismatch recognition and uracil excision provide complementary paths to both Ig switching and the A/T-focused phase of somatic mutation. Mol. Cell. 16, 163-171. (doi:10.1016/j.molcel.2004.10.011)
38. Rajewsky, K., Forster, I. & Cumano, A. 1987 Evolutionary and somatic selection of the antibody repertoire in the mouse. Science 238, 1088-1094. (doi:10.1126/science.3317826)
39. Rogozin, I. B., Basu, M. K., Jordan, I. K., Pavlov, Y. I. & Koonin, E. V. 2005 APOBEC4, a new member of the AID/APOBEC family of polynucleotide (deoxy)cytidine deaminases predicted by computational analysis. Cell Cycle 4, 1281-1285.
40. Sheehy, A. M., Gaddis, N. C., Choi, J. D. & Malim, M. H. 2002 Isolation of a human gene that inhibits HIV-1 infection and is suppressed by the viral Vif protein. Nature 418, 646-650. (doi:10.1038/nature00939)
41. Shen, H. M. & Storb, U. 2004 Activation-induced cytidine deaminase (AID) can target both DNA strands when the DNA is supercoiled. Proc. Natl Acad. Sci. USA 101, 12 997-13 002. (doi:10.1073/pnas.0404974101)
42. Shinkura, R., Okazaki, I. M., Muto, T., Begum, N. A. & Honjo, T. 2007 Regulation of AID function in vivo. Adv. Exp. Med. Biol. 596, 71-81. (doi:10.1007/0-387-46530-8-7)
43. Sohail, A., Klapacz, J., Samaranayake, M., Ullah, A. & Bhagwhat, A. S. 2003 Human activation-induced cytidine deaminase causes transcription- dependent, strand-biased C to U deaminations. Nucl. Acids Res. 31, 2990-2994. (doi:10.1093/nar/gkg464)
44. Stanford, N. P., Szczelkun, M. D., Marko, J. F. & Halford, S. E. 2000 One- and three-dimensional pathways for proteins to reach specific DNA sites. EMBO J. 19, 6546-6557. (doi:10.1093/emboj/19.23.6546)
45. Stavnezer, J., Guikema, J. E. & Schrader, C. E. 2008 Mechanism and regulation of class switch recombination. Annu. Rev. Immunol. 26, 261-292. (doi:10.1146/annurev.immunol.26.021607.090248)
46. Suspene, R., Sommer, P., Henry, M., Ferris, S., Guetard, D., Pochet, S., Chester, A., Navaratnam, N., Wain-Hobson, S. & Vartanian, J. P. 2004 APOBEC3G is a single-stranded DNA cytidine deaminase and functions independently of HIV reverse transcriptase. Nucleic Acids Res. 32, 2421-2429. (doi:10.1093/nar/gkh554)
47. Suspene, R., Rusniok, C., Vartanian, J. P. & Wain-Hobson, S. 2006 Twin gradients in APOBEC3 edited HIV-1 DNA reflect the dynamics of lentiviral replication. Nucleic Acids Res. 34, 4677-4684. (doi:10.1093/nar/gkl555)
48. Terry, B. J., Jack, W. E. & Modrich, P. 1985 Facilitated diffusion during catalysis by EcoRI endonuclease. Nonspecific interactions in EcoRI catalysis. J. Biol. Chem. 260, 13 130-13 137.
49. Vartanian, J. P., Guetard, D., Henry, M. & Wain-Hobson, S. 2008 Evidence for editing of human papillomavirus DNA by APOBEC3 in benign and precancerous lesions. Science 320, 230-233. (doi:10.1126/science. 1153201)
50. von Hippel, P. H. & Berg, O. G. 1989 Facilitated target location in biological systems. J. Biol. Chem. 264, 675-678.
51. Yu, Q., Konig, R., Pillai, S., Chiles, K., Kearney, M., Palmer, S., Richman, D., Coffin, J. M. & Landau, N. R. 2004 Single-strand specificity of APOBEC3G accounts for minus-strand deamination of the HIV genome. Nat. Struct. Mol. Biol. 11, 435-442. (doi:10.1038/nsmb758)
52. Zhu, Y., Nonoyama, S., Morio, T., Muramatsu, M., Honjo, T. & Mizutani, S. 2003 Type two hyper-IgM syndrome caused by mutation in activation-induced cytidine deaminase. J. Med. Dent. Sci. 50, 41-46.